Mobility and distribution of boron in plants and effects on reproductive growth and yield

Öz

Most boron (B) behaviour in plants can be explained by complexation of B in cell walls and membranes which links the consequences of B deficiency to the disruption of cell wall and membrane function. Many symptoms of B deficiency reflect the localised and timely need for B for stabilisation of cell walls in tissues with expanding cells, e.g. flowers, fruit, root tips and shoot meristems. The internal B requirement of tissues for adequate function is determined by the abundance of rhamnogalacturonan-II (RG-II) which complexes B in the cell wall. Reproductive plant parts appear to be particularly at risk from low B supply, in part because they require relatively high concentrations of B compared to vegetative tissues.  When external B concentrations are adequate to high, the uptake and distribution of B in plants can be largely explained by the uptake of water and its movement within the plant. However, under marginal and deficient external B concentrations, channels and transporters exert significant control of the uptake and distribution of B within the plant. Channels and transporters in roots promote uptake and loading of B into the xylem. For flowers, pollen and seed, with low rates of transpiration, channels and transporters are probably involved in their B acquisition under low external supply. The mobility of B in the phloem is variable among species. In most plants, B is immobile in the phloem and growing tissues rely substantially on B supplied through the xylem or by xylem-to-phloem transfer. However, if present in the phloem, B-complexing compounds, notably sugar alcohols, allow free mobility of B in the phloem so that B can be retranslocated within the plant of those species especially under deficient supply. 

Anahtar Kelimeler

• Boron-complexing,Boron requirements,Cell wall,Deficiency symptoms,Pectin,RG-II,Sugar alcohols

Kaynakça

1. [1] Dell B., Brown P. H., Bell, R. W. (Editors), Boron in Soils and Plants: Reviews, Developments in Plant and Soil Sciences Vol. 77. Kluwer Academic Publishers, Dordrecht, The Netherlands. p. 219. 1997. [2] Goldbach H. E., Rerkasem B., Wimmer M. A., Brown P. H., Thellier M., Bell R.W. (Editors), Boron in Plant and Animal Nutrition, Kluwer Academic Publishers, Dordrecht, The Netherlands. p. 410. 2002.
2. [3] Xu F., Goldbach H. E., Brown P. H., Bell, R. W., Fujiwara, T. Hunt, C. D., Goldberg S. Shi L. (Eds), Advances in Plant and Animal Boron Nutrition, Springer, Dordrecht. pp. 401. 2007.
3. [4] Reid R., Understanding the boron transport network in plants, Plant and Soil 385, 1–13. 2014. [5] Matoh T., Boron in plant cell wall, Plant and Soil 193, 59–70. 1997.
4. [6] O’Neill, M. A., Ishii, T., Albersheim, P. and Darvill, A. G., Rhamnogalacturonan II: Structure and function of a borate cross-linked cell wall pectic polysaccharide, Annual Review of Plant Biology 55, 109-139. 2004.
5. [7] Warington K., The effect of boric acid and borax on the broad bean and certain other plants, Annals of Botany 37, 629–672. 1923.
6. [8] Epstein E., Mineral Nutrition of Plants: Principles and Perspectives. J. Willey and Sons, New York. 1972.
7. [9] Brown P. H., Bellaloui N., Wimmer M. A., Bassil E., Ruiz J., Hu H., et al., Boron in plant biology, Plant Biol., 4, 205–223. 2002 doi:10.1055/s-2002-2574 [10] Wimmer M. A., Lochnit G., Bassil E., Muhling K. H., Goldbach H. E., Membrane-associated, boron-interacting proteins isolated by boronate affinity chromatography, Plant Cell Physiol., 50, 1292–1304. 2009.
8. [11] Voxeur A., Fry S. C., Glycosylinositol phosphorylceramides from Rosa cell cultures are boron-bridged in the plasma membrane and form complexes with rhamnogalacturonan, II. Plant J.,l 79, 139-149, 2014.

9. [12] Loomis W., Durst, R., Chemistry and biology of boron, BioFactors, 3, 229-239. 1992. [13] Chormova D., Messenger D. J., Fry S. C., Boron bridging of rhamnogalacturonan-II, monitored by gel electrophoresis, occurs during polysaccharide synthesis and secretion but not post-secretion, The Plant J., 77, 534–546, 2014.
10. [14] Hu H., Brown P. H., Labavitch J. M., Species variability in boron requirement is correlated with cell wall pectin, J. Exp. Bot., 47, 227–232, 1996.
11. [15] Huang L., Pant J., Bell R.W., Dell B., Deane K., Effects of boron deficiency and low temperature on wheat sterility, In: Sterility in Wheat in Sub-tropical Asia: Extent, Causes and Solutions, Eds H.M. Rawson and K.D. Subedi. pp. 90-102. ACIAR Proceedings No. 72. 1996.
12. [16] Kirk G. J., Loneragan J. F., Functional boron requirement for leaf expansion and its use as a critical value for diagnosis of boron deficiency in soybean, Agron. J., 80, 758–762, 1988.
13. [17] Bell R. W., McLay L. D., Plaskett D., Dell B., Loneragan J. F., Germination and vigour of black gram (Vigna mungo L. Hepper) seed from plants grown with and without boron, Aust. J. Agric. Res., 40, 273–279. 1989.
14. [18] Bell R. W., Rerkasem B., Keerati-Kasikorn P., Phetchawee S., Hiranburana N., Ratanarat S., Pongsakul P., Loneragan J. F., Mineral Nutrition of Food Legumes in Thailand with particular reference to micronutrients, ACIAR Technical Report 19, pp. 52, 1990.
15. [19] Rerkasem B., Bell R. W., Loedkaew S., Loneragan J. F., Boron deficiency in soybean [Glycine max (L.) Merr.], peanut (Arachis hypogaea L.) and black gram [Vigna mungo (L.) Hepper]: Symptoms in seeds and differences among soybean cultivars in susceptibility to boron deficiency, Plant Soil 150, 289–294. 1993.
16. [20] Rerkasem B., Lordkaew S., Dell B., Boron requirement for reproductive development in wheat, Soil Sci. Plant Nutr., 43, 953–957, 1997.
17. [21] Rerkasem B., Loneragan J. F., Boron deficiency in two wheat genotypes in a warm, subtropical region, Agron. J., 86, 887–890. 1994. [22] Rerkasem B., Bell R. W., Lordkaew S., Loneragan J. F. Relationship of seed boron concentration to germination and growth of soybean (Glycine max L. Merr.), Nutr. Cycling Agroecosyst., 48, 217-223, 1997.
18. [23] Lordkaew S., Konsaeng S., Jongjaidee J., Dell B., Rerkasem B., Jamjod S., Variation in responses to boron in rice, Plant Soil, 363, 287-295, 2011.
19. [24] Asad A., Bell R. W., Dell B., Huang L., External boron requirements of canola in boron buffered solution culture system, Ann. Bot., 80, 65-73, 1997. [25] Asad A., Bell R.W., Dell B., Uptake and distribution of boron in canola at vegetative and early flowering stages using boron buffered solution culture, Commun. Soil Sci. Plant Anal., 31, 2233-2249, 2000. [26] Asad A., Bell R. W., Dell B., A critical comparison of the external and internal boron requirements for contrasting species in boron-buffered solution culture., Plant Soil 233, 31-45, 2001. [27] Dell B., Huang L., Physiological response of plants to low boron, Plant Soil, 193, 103-120, 1997.
20. [28] Huang L., Pant J., Dell B. Bell R. W., Effects of boron deficiency on anther development and floret fertility in wheat (Triticum aestivum L. cv. Wilgoyne), Ann. Bot., 85, 493-500, 2000.
21. [29] Rawson H. M., Hypothesis for why sterility occurs in wheat in Asia. pp. 132-134, In: H.M. Rawson and K.D. Subedi (eds.), Sterility in Wheat in Sub-tropical Asia: Extent, Causes and Solutions, ACIAR Proc. No. 72. 1996.
22. [30] Huang L., Dell B., Bell R. W., Seasonal conditions modify pollen viability responses to B deficiency in wheat (Triticum aestivum L. cv. Wilgoyne), In Boron in Plant and Animal Nutrition, H.E. Goldbach, B. Rerkasem, M.A. Wimmer, P.H. Brown, M. Thellier and R.W. Bell. eds. pp. 137-141. Kluwer Academic Publishers, Dordrecht, The Netherlands. 2002. [31] Agarwala S. C., Sharma P. N., Chatterjee C., Sharma C. P., Development and enzymatic changes during pollen development in boron deficient maize plants, J. Plant Nutr., 3, 329–336, 1981. [32] Wimmer M. A., Eichert T., Review: Mechanisms for boron deficiency-mediated changes in plant water relations, Plant Sci., 203-204, 25-32, 2013.
23. [33] Yoshinari A., Takano J., Insights into the mechanisms underlying boron homeostasis in plants: Mini Review, Frontier in Plant Science 8, Article 1951 November 2017.
24. [34] Shao J. F., Yamaji N., Ma, J. F., Preferential distribution of boron to developing tissues is mediated by OsNIP3;1 located in rice node, In Proceedings of the XVIII International Plant Nutrition Colloquium, 21 - 24 August 2017, Satellite Meetings 19 - 20 August, Copenhagen• Denmark. Proceedings Book. Eds A. Carstensen, K.H. Laursen and J.K. Schjørring. www.ipnc2017.org 2017.
25. [35] Huang L., Bell R. W., Dell B., Boron supply to wheat (Triticum aestivum L. cv. Wilgoyne) ear during early growth phase, J. Exp. Bot., 52, 1731-1738, 2001.
26. [36] Shelp B. J., Kitheka A. M, Vanderpool R. A., Spiers G. A., Xylem-to-phloem transfer of boron in broccoli and lupin during early reproductive growth, Physiol. Plant., 104, 533-540, 1998.
27. [37] Chatterjee M., Tabi Z., Galli M., Malcomber S., Buck A., Muszynski M., Gallavotti A., The boron efflux transporter ROTTEN EAR Is required for maize inflorescence development and fertility, The Plant Cell 26, 2962–2977, 2014.
28. [38] Brown P. H., Hu H., Phloem mobility of boron is species dependent: Evidence for phloem mobility in sorbitol-rich species, Ann. Bot., 77, 497–506, 1996. [39] Huang L., Bell R.W., Dell B., Evidence of phloem boron transport in response to interrupted boron supply in white lupin (Lupinus albus L. cv. Kiev Mutant) at the reproductive stage, J. Exp. Bot. 59, 575–583, 2008. [40] Konsaeng S., Dell B., Rerkasem B., Boron mobility in peanut (Arachis hypogaea L.), Plant Soil, 330, 281–289, 2010.
29. [41] Stangoulis J. C. R., Brown P. H., Bellaloui N., Reid R. J., Graham R. D., The efficiency of boron utilisation in canola, Aust. J. Plant Physiol., 28, 1109-1114, 2001.
30. [42] Lehto T., Räisänen M., Lavola A., Julkunen-Tiitto R., Aphalo P. J. Boron mobility in deciduous forest trees in relation to their polyols, New Phytol., 163, 333-339, 2004.
31. [43] Stangoulis J., Tate M., Graham R., Bucknall M., Palmer L., Boughton B., Reid R., The mechanism of boron mobility in wheat and canola phloem, Plant Physiol., 153, 876–881, 2010.
32. [44] Wang N., Yang C., Pan Z., Liu Y., Peng S., Boron deficiency in woody plants: Various responses and tolerance mechanisms, Front. Plant Sci., 6, 916, 1-14, 2015.
33. [45] Brown P. H., Bellaloui N., Hu H., Dandekar A., Transgenically enhanced sorbitol synthesis facilitates phloem boron transport and increases tolerance of tobacco to boron deficiency, Plant Physiol, 119, 17–20, 1999. [46] Nachiangmai D., Dell B., Bell R. W., Huang L., Rerkasem B., Enhanced boron transport into the ear of wheat as a mechanism for boron efficiency Plant Soil 264, 141-147, 2004.
34. [47] Pant J., Rerkasem B., Noppakoonwong R., Effect of water stress on the boron response of wheat genotypes under low boron field conditions, Plant Soil 202, 193–200, 1998. [48] Huang L., Gherardi M., Bell R. W., Dell B., High light intensity increases external B requirements for leaf growth of sunflower (Helianthus annuus L. cv. Hysun 25) in boron-buffered (B) solution culture, In Boron in Plant and Animal Nutrition. H.E. Goldbach, B. Rerkasem, M.A. Wimmer, P.H. Brown, M. Thellier and R.W. Bell. eds. pp. 213-225. Kluwer Academic Publishers, Dordrecht, 2002.
35. [49] Eichert T., Goldbach H. E., Transpiration rate affects the mobility of foliar-applied boron in Ricinus communis L. cv. Impala, Plant Soil, 328, 165–174, 2010.
36. [50] Ye Z. Q., Bell R. W., Dell B., Huang H., Response of sunflower (Helianthus annuus L.) to boron supply at low root zone temperature, Commun. Soil Sci. Plant Anal., 31, 2379-2392, 2000.
37. [51] Ye Z. Q., Huang L., Bell R. W., Dell B., Low root zone temperature favours shoot B partitioning into young leaves of oilseed rape (Brassica napus L. cv Hyola 42), Physiol. Plant., 118, 213-220, 2003.
38. [52] Ye Z. Q., Bell R. W., Dell B., Huang L., Xu Q., Effects of root zone temperature on oilseed rape (Brassica napus) response to boron, Commun. Soil Sci. Plant Anal., 37, 2791-2803, 2006.
39. [53] Abat M., Degryse F., Baird R., McLaughlin M. J., Responses of canola (Brassica napus L.) to the application of slow-release boron fertilizers and their residual effect, Soil Sci. Soc. Am. J., 79, 97-. 2015.
40. [54] Bell R. W., Dell B., Micronutrients in Sustainable Food, Feed, Fibre and Bioenergy Production, IFA, Paris, 2008. [55] Nyomora A. M. S., Brown P. H., Freeman M., Fall foliar-applied boron increases tissue boron concentration and nut set in almond, J. Am. Soc. Hortic. Sci., 22, 405-410, 1997.
41. [56] Bell R. W., Temporary nutrient deficiency - a difficult case for diagnosis and prognosis by plant analysis, Commun. Soil Sci. Plant Anal., 31, 1847-1861, 2000. [57] Nyomora A. M., Brown P. H., Krueger B., Rate and time of boron application increase almond productivity and tissue boron concentration HortSci., 34, 242-245, 1999.